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Sema3A and neuropilin-1 expression and distribution in rat white adipose tissue

  • Published:
Journal of Neurocytology

Abstract

Semaphorins are cell surface and/or soluble signals that exert an inhibitory control on axon guidance. Sema3A, the vertebrate-secreted semaphorin, binds to neuropilin-1, which together with plexins constitutes the functional receptor. To verify whether Sema3A is produced by white adipocytes and, in that case, to detect its targets in white adipose tissue, we studied the cell production and tissue distribution of Sema3A and neuropilin-1 in rat retroperitoneal and epididymal adipose depots. Sema3A and neuropilin-1 were detected in these depots by Western blotting. The immunohistochemical results showed that Sema3A is produced in, and possibly secreted by, smooth muscle cells of arteries and white adipocytes. Accordingly, neuropilin-1 was found on perivascular and parenchymal nerves. Such a pattern of distribution is in line with a role for secreted Sema3A in the growth and plasticity of white adipose tissue nerves. Indeed, after fasting, when white adipocytes are believed to be overstimulated by noradrenaline and rearrangement of the parenchymal nerve supply may occur, adipocytic expression of Sema3A is reduced. Finally, the presence of neuropilin-1 in some white adipocytes raises the interesting possibility that Sema3A also exerts an autocrine-paracrine role on these cells.

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References

  • BARTNESS, T. J. & BAMSHAD, M. (1998) Innervation of mammalian white adipose tissue: Implications for the regulation of total body fat. American Journal of Physiology 275, R1399–1411.

    Google Scholar 

  • BEHAR, O., GOLDEN, J. A., MASHIMO, H., SCHOEN, F. J. & FISHMAN, M. C. (1996) Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383, 525–528.

    Google Scholar 

  • BRADFORD, M. M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein Sema3A-sensitive nerves in white adipose tissue 351 utilizing the principle of protein-dye binding. Analytical Biochemistry 71, 248–254.

    Google Scholar 

  • CHEN, H., HE, Z., BAGRI, A. & TESSIER-LAVIGNE, M. (1998) Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 21, 1283–1290.

    Google Scholar 

  • CINTI, S. (1999) The Adipose Organ. Milan: Editrice Kurtis.

    Google Scholar 

  • CINTI, S. (2001) The adipose organ: Morphological perspectives of adipose tissues. Proceedings of the Nutrition Society 60, 319–328.

    Google Scholar 

  • CUI, J. & HIMMS-HAGEN, J. (1992) Rapid but transient atrophy of brown adipose tissue in capsaicin-desensitized rats. American Journal of Physiology 262, R562–R567.

    Google Scholar 

  • DE MATTEIS, R., RICQUIER, D. & CINTI, S. (1998) TH-, NPY-, SP-, and CGRP-immunoreactive nerves in interscapular brown adipose tissue of adult rats acclimated at different temperatures: An immunohistochemical study. Journal of Neurocytology 27, 877–886.

    Google Scholar 

  • DI GIROLAMO, M., SKINNER, N. S. Jr, HANLEY, H. G. & SACHS, R. G. (1971) Relationship of adipose tissue blood flow to fat cell size and number. American Journal of Physiology 220, 932–937.

    Google Scholar 

  • GAROFALO, M. A., KETTELHUT, I. C., ROSELINO, J. E. & MIGLIORINI, R. H. (1996) Effect of acute cold exposure on norepinephrine turnover in rat white adipose tissue. Journal of the Autonomic Nervous System 60, 206–208.

    Google Scholar 

  • GAVAZZI, I. (2001) Semaphorin-neuropilin-1 interactions in plasticity and regeneration of adult neurons. Cell & Tissue Research 305, 275–284.

    Google Scholar 

  • GILGEN, A., MAICKEL, R. P., NIKOULINA, S. E. & BRODIE, B. B. (1962) Essential role of catecholamines in the mobilisation of free fatty acids and glucose after cold exposure. Life Science 1, 709–715.

    Google Scholar 

  • GIORDANO, A., MORRONI, M., SANTONE, G., MARCHESI, G. F. & CINTI, S. (1996) Tyrosine hydroxylase, neuropeptide Y, substance P, calcitonin gene-related peptide and vasoactive intestinal peptide in nerves of rat periovarian adipose tissue: An immunohistochemical and ultrastructural investigation. Journal of Neurocytology 25, 125–136.

    Google Scholar 

  • GIORDANO, A., MORRONI, M., CARLE, F., GESUITA, R., MARCHESI, G. F. & CINTI, S. (1998) Sensory nerves affect the recruitment and differentiation of rat periovarian brown adipocytes during cold acclimation. Journal of Cell Science 111, 2587–2594.

    Google Scholar 

  • GIORDANO, A., COPPARI, R., CASTELLUCCI, M. & CINTI, S. (2001) Sema3a is produced by brown adipocytes and its secretion is reduced following cold acclimation. Journal of Neurocytology 30, 5–10.

    Google Scholar 

  • GOSHIMA, Y., TAKAAKI, I., SASAKI, Y. & NAKAMURA, F. (2002) Semaphorins as signals for cell repulsion and invasion. Journal of Clinical Investigation 109, 993–998.

    Google Scholar 

  • HE, Z. & TESSIER-LAVIGNE, M. (1997) Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell 90, 739–751.

    Google Scholar 

  • ITO, T., KAGOSHIMA, M., SASAKI, Y., LI, C., UDAKA, N., KITSUKAWA, T., FUJISAWA, H., TANIGUCHI, M., YAGI, T., KITAMURA, H. & GOSHIMA, Y. (2000) Repulsive axon guidance molecule Sema3A inhibits branching morphogenesis of fetal mouse lung. Mechanisms in Development 97, 35–45.

    Google Scholar 

  • KAWASAKI, T., BEKKU, Y., SUTO, F., KITSUKAWA, T., TANIGUCHI, M., NAGATSU, I., NAGATSU, T., ITOH, K., YAGI, T. & FUJISAWA, H. (2002) Requirement of neuropilin 1-mediated Sema3A signals in patterning of the sympathetic nervous system. Development 129, 671–680.

    Google Scholar 

  • KITSUKAWA, T., SHIMIZU, M., SANBO, M., HIRATA, T., TANIGUCHI, M., BEKKU, Y., YAGI, T. & FUJISAWA, H. (1997) Neuropilin-semaphorin III/Dmediated chemorepulsive signals play a crucial role in peripheral nerve projections in mice. Neuron 19, 995–1005.

    Google Scholar 

  • KOLODKIN, A. L., LEVENGOOD, D. V., ROWE, E. G., TAI, Y. T., GIGER, R. J. & GINTY, D. D. (1997) Neuropilin is a semaphorin III receptor. Cell 90, 753–762.

    Google Scholar 

  • KOLODKIN, A. L. (1998) Semaphorin-mediated neuronal growth cone guidance. Progress in Brain Research 117, 115–132.

    Google Scholar 

  • LAEMMLI, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.

    Google Scholar 

  • LUO, Y., RAIBLE, D. & RAPER, J. A. (1993) Collapsin: A protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217–227.

    Google Scholar 

  • MA, S. W. & FOSTER, D. O. (1986) Starvation-induced changes in metabolic rate, blood flow, and regional energy expenditure in rats. Canadian Journal of Physiology & Pharmacology 64, 1252–1258.

    Google Scholar 

  • MIGLIORINI, R. H., GAROFALO, M. A. & KETTELHUT, I. C. (1997) Increased sympathetic activity in rat white adipose tissue during prolonged fasting. American Journal of Physiology 272, R656–R661.

    Google Scholar 

  • RAYNER, D. V. (2001) The sympathetic nervous system in white adipose tissue regulation. Proceedings of the Nutrition Society 60, 357–364.

    Google Scholar 

  • REBUFFE'-SCRIVE, M. (1991) Neuroregulation of adipose tissue: Molecular and hormonal mechanisms. International Journal of Obesity 15, 83–86.

    Google Scholar 

  • ROBERT, B., ZHAO, X. & ABRAHAMSON, D. R. (2000) Coexpression of neuropilin-1, Flk1, and VEGF(164) in developing and mature mouse kidney glomeruli. American Journal of Physiology 279, F275–F282.

    Google Scholar 

  • SEMAPHORIN NOMENCLATURE COMMITTEE (1999) Unified nomenclature for the semaphorins/collapsins. Cell 97, 551–552.

    Google Scholar 

  • SLAVIN, B. G. & BALLARD, K. W. (1978) Morphological studies on the adrenergic innervation of white adipose tissue. Anatomical Record 191, 377–389.

    Google Scholar 

  • SOKER, S., TAKASHIMA, S., MIAO, H. Q., NEUFELD, G. & KLAGSBRUN, M. (1998) Neuropilin-1 is expressed by endothelial and tumour cells as and isoformspecific receptor for vascular endothelial growth factor. Cell 92, 735–745.

    Google Scholar 

  • TAMAGNONE, L. & COMOGLIO, P. M. (2000) Signalling by semaphorin receptors: Cell guidance and beyond. Trends in Cell Biology 10, 377–383.

    Google Scholar 

  • TANELIAN, D. L., BARRY, M. A., JOHNSTON, S. A., LE, T. & SMITH, G. M. (1997) Semaphorin III can repulse and inhibit adult sensory afferents in vivo. Nature Medicine 3, 1398–1401.

    Google Scholar 

  • THOMPSON, R. J., DORAN, J. F., JACKSON, P., DHILLON, A. P. & RODE, J. (1983) PGP 9.5-a new marker for vertebrate neurons and neuroendocrine cells. Brain Research 278, 224–228.

    Google Scholar 

  • VAN VACTOR, D. V. & LORENZ, L. J. (1999) Neural development: The semantics of axon guidance. Current Biology 9, 201–204.

    Google Scholar 

  • WILSON, P. O. G., BARBER, P. C., HAMID, Q. A., POWER, B. F., DHILLON, A. P., RODE, J., DAY, I. N. M., THOMPSON, R. J. & POLAK, J. M. (1988) The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. British Journal of Experimental Pathology 69, 91–104.

    Google Scholar 

  • WRIGHT, D. E., WHITE, F. A., GERFEN, R. W., SILOSSANTIAGO, I. & SNIDER, W. D. (1995) The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. Journal of Comparative Neurology 361, 321–333.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Normal Human Morphology, Marche Polytechnic University, Ancona, Italy

    Antonio Giordano, Paola Cesari, Lorena Capparuccia, Mario Castellucci & Saverio Cinti

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  1. Antonio Giordano
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  2. Paola Cesari
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  3. Lorena Capparuccia
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  4. Mario Castellucci
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  5. Saverio Cinti
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Correspondence to Saverio Cinti.

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Giordano, A., Cesari, P., Capparuccia, L. et al. Sema3A and neuropilin-1 expression and distribution in rat white adipose tissue. J Neurocytol 32, 345–352 (2003). https://doi.org/10.1023/B:NEUR.0000011328.61376.bb

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  • DOI: https://doi.org/10.1023/B:NEUR.0000011328.61376.bb

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